Effects of BAFF Neutralization on Atherosclerosis Associated With Systemic Lupus Erythematosus

Arthritis Rheumatol. 2021 Feb;73(2):255-264. doi: 10.1002/art.41485. Epub 2020 Dec 15.

Abstract

Objective: Cardiovascular disease (CVD) is the leading cause of death in systemic lupus erythematosus (SLE). B cells play a key role in the pathogenesis of lupus, and anti-BAFF therapy has been approved for use in SLE. Since mature B cells also promote atherosclerosis, we undertook this study to evaluate, in a mouse model and in SLE patients, whether BAFF neutralization has an atheroprotective effect in SLE.

Methods: The effect of BAFF on atherosclerosis associated with lupus was investigated in the atherosclerosis/lupus-prone apolipoprotein E-knockout D227K mouse model and in a cohort of SLE patients. Mice were treated with a blocking anti-BAFF monoclonal antibody (mAb), while fed a standard chow diet. Carotid plaque and carotid intima-media thickness were assessed by ultrasound at baseline and during follow-up in SLE patients who were asymptomatic for CVD.

Results: Anti-BAFF mAb in ApoE-/- D227K mice induced B cell depletion, efficiently treated lupus, and improved atherosclerosis lesions (21% decrease; P = 0.007) in mice with low plasma cholesterol levels but worsened the lesions (17% increase; P = 0.06) in mice with high cholesterol levels. The atheroprotective effect of the BAFF-BAFF receptor signaling inhibition on B cells was counterbalanced by the proatherogenic effect of the BAFF-TACI signaling inhibition on macrophages. In SLE patients, blood BAFF levels were associated with subclinical atherosclerosis (r = 0.26, P = 0.03). Anti-BAFF mAb treatment had a differential effect on the intima-media thickness progression in SLE patients depending on body mass index.

Conclusion: Depending on the balance between lipid-induced and B cell-induced proatherogenic conditions, anti-BAFF could be detrimental or beneficial, respectively, to atherosclerosis development in SLE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Adventitia / pathology
  • Animals
  • Antibodies, Neutralizing / pharmacology
  • Aorta / pathology
  • Atherosclerosis / diagnostic imaging
  • Atherosclerosis / immunology
  • Atherosclerosis / metabolism*
  • B-Cell Activating Factor / antagonists & inhibitors*
  • B-Cell Activating Factor / metabolism*
  • B-Lymphocytes / immunology*
  • Carotid Artery Diseases / diagnostic imaging
  • Carotid Artery Diseases / metabolism
  • Carotid Intima-Media Thickness
  • Cell Proliferation
  • Cholesterol / metabolism*
  • Female
  • Foam Cells / drug effects
  • Foam Cells / metabolism
  • Humans
  • Lupus Erythematosus, Systemic / immunology
  • Lupus Erythematosus, Systemic / metabolism*
  • Male
  • Mice
  • Mice, Knockout, ApoE
  • Middle Aged
  • Phenotype
  • Plaque, Atherosclerotic / diagnostic imaging
  • Plaque, Atherosclerotic / metabolism
  • Signal Transduction
  • Transmembrane Activator and CAML Interactor Protein / metabolism*
  • Ultrasonography

Substances

  • Antibodies, Neutralizing
  • B-Cell Activating Factor
  • TNFSF13B protein, human
  • Tnfsf13b protein, mouse
  • Transmembrane Activator and CAML Interactor Protein
  • Cholesterol